Repeat-sequence turnover shifts fundamentally in species with large genomes
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
PubMed
33077876
DOI
10.1038/s41477-020-00785-x
PII: 10.1038/s41477-020-00785-x
Knihovny.cz E-zdroje
- MeSH
- cykasy genetika MeSH
- fylogeneze MeSH
- genom rostlinný genetika MeSH
- Magnoliopsida genetika MeSH
- průtoková cytometrie MeSH
- repetitivní sekvence nukleových kyselin genetika MeSH
- retroelementy genetika MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- retroelementy MeSH
Given the 2,400-fold range of genome sizes (0.06-148.9 Gbp (gigabase pair)) of seed plants (angiosperms and gymnosperms) with a broadly similar gene content (amounting to approximately 0.03 Gbp), the repeat-sequence content of the genome might be expected to increase with genome size, resulting in the largest genomes consisting almost entirely of repetitive sequences. Here we test this prediction, using the same bioinformatic approach for 101 species to ensure consistency in what constitutes a repeat. We reveal a fundamental change in repeat turnover in genomes above around 10 Gbp, such that species with the largest genomes are only about 55% repetitive. Given that genome size influences many plant traits, habits and life strategies, this fundamental shift in repeat dynamics is likely to affect the evolutionary trajectory of species lineages.
Biology Centre Czech Academy of Sciences České Budějovice Czech Republic
Division of Molecular Biology Department of Biology University of Zagreb Zagreb Croatia
Guangzhou University of Chinese Medicine Guangzhou China
Institut Botànic de Barcelona Barcelona Spain
Institute of Biophysics Academy of Sciences of the Czech Republic Brno Czech Republic
Jodrell Laboratory Royal Botanic Gardens Kew Richmond UK
School of Biological and Chemical Sciences Queen Mary University of London London UK
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Lisch, D. How important are transposons for plant evolution? Nat. Rev. Genet. 14, 49–61 (2013).
Bennetzen, J. L. & Park, M. Distinguishing friends, foes, and freeloaders in giant genomes. Curr. Opin. Genet. Dev. 49, 49–55 (2018).
Kersey, P. J. Plant genome sequences: past, present, future. Curr. Opin. Plant Biol. 48, 1–8 (2019).
Elliott, T. A. & Gregory, T. R. What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Phil. Trans. Roy. Soc. B 370, 20140331 (2015).
Elliott, T. A. & Gregory, T. R. Do larger genomes contain more diverse transposable elements? BMC Evol. Biol. 15, 69 (2015).
Neumann, P., Novák, P., Hoštáková, N. & Macas, J. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob. DNA 10, 1 (2019).
Mabuchi, T., Kokubun, H., Mii, M. & Ando, T. Nuclear DNA content in the genus Hepatica (Ranunculaceae). J. Plant Res. 118, 37–41 (2005).
Nowoshilow, S. et al. The axolotl genome and the evolution of key tissue formation regulators. Nature 554, 50–55 (2018).
Stritt, C., Wyler, M., Gimmi, E. L., Pippel, M. & Roulin, A. C. Diversity, dynamics and effects of long terminal repeat retrotransposons in the model grass Brachypodium distachyon. New Phytol. 227, 1736–1748 (2020).
Ma, J. X. & Bennetzen, J. L. Recombination, rearrangement, reshuffling, and divergence in a centromeric region of rice. Proc. Natl Acad. Sci. USA 103, 383–388 (2006).
Neumann, P., Koblížková, A., Navrátilová, A. & Macas, J. Significant expansion of Vicia pannonica genome size mediated by amplification of a single type of giant retroelement. Genetics 173, 1047–1056 (2006).
Nystedt, B. et al. The Norway spruce genome sequence and conifer genome evolution. Nature 497, 579–584 (2013).
De La Torre, A. R., Li, Z., Van de Peer, Y. & Ingvarsson, P. K. Contrasting rates of molecular evolution and patterns of selection among gymnosperms and flowering plants. Mol. Biol. Evol. 34, 1363–1377 (2017).
Metcalfe, C. J., Filée, J., Germon, I., Joss, J. & Casane, D. Evolution of the Australian lungfish (Neoceratodus forsteri) genome: a major role for CR1 and L2 LINE elements. Mol. Biol. Evol. 29, 3529–3539 (2012).
Sun, C., López Arriaza, J. R. & Mueller, R. L. Slow DNA loss in the gigantic genomes of salamanders. Genome Biol. Evol. 4, 1340–1348 (2012).
Vu, G. T. H., Cao, H. X., Reiss, B. & Schubert, I. Deletion-bias in DNA double-strand break repair differentially contributes to plant genome shrinkage. New Phytol. 214, 1712–1721 (2017).
Tiley, G. P. & Burleigh, J. G. The relationship of recombination rate, genome structure, and patterns of molecular evolution across angiosperms. BMC Evol. Biol. 15, 194 (2015).
Kent, T. V., Uzunović, J. & Wright, S. I. Coevolution between transposable elements and recombination. Philos. Trans. Roy. Soc. B 372, 20160458 (2017).
Maumus, F. & Quesneville, H. Deep investigation of Arabidopsis thaliana junk DNA reveals a continuum between repetitive elements and genomic dark matter. PLoS ONE 9, e94101 (2014).
Kelly, L. J. et al. Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size. New Phytol. 208, 596–607 (2015).
Bennetzen, J. L. & Kellogg, E. A. Do plants have a one-way ticket to genomic obesity? Plant Cell 9, 1509–1514 (1997).
Leitch, A. R. & Leitch, I. J. Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol. 194, 629–646 (2012).
Francis, D., Davies, M. S. & Barlow, P. B. A strong nucleotypic effect of DNA C-value on the cell cycle regardless of ploidy level. Ann. Bot. 101, 747–757 (2008).
Doyle, J. J. & Coate, J. E. Polyploidy, the nucleotype, and novelty: the Impact of genome doubling on the biology of the cell. Int. J. Plant Sci. 180, 1–52 (2019).
Roddy, A. B. et al. The scaling of genome size and cell size limits maximum rates of photosynthesis with implications for ecological strategies. Int. J. Plant Sci. 181, 75–87 (2020).
Lawson, T. & Blatt, M. R. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol. 164, 1556–1570 (2014).
Franks, P. J. & Beerling, D. J. Maximum leaf conductance driven by CO
Pellicer, J., Hidalgo, O., Dodsworth, S. & Leitch, I. J. Genome size diversity and its impact on the evolution of land plants. Genes 9, 88 (2018).
Knight, C. A., Molinari, N. A. & Petrov, D. A. The large genome constraint hypothesis: evolution, ecology and phenotype. Ann. Bot. 95, 177–190 (2005).
Vidic, T., Greilhuber, J., Vilhar, B. & Dermastia, M. Selective significance of genome size in a plant community with heavy metal pollution. Ecol. Appl. 19, 1515–1521 (2009).
Fleischmann, A. et al. Evolution of genome size and chromosome number in the carnivorous plant genus Genlisea (Lentibulariaceae), with a new estimate of the minimum genome size in angiosperms. Ann. Bot. 114, 1651–1663 (2014).
Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017).
Landis, J. B. et al. Impact of whole-genome duplication events on diversification rates in angiosperms. Am. J. Bot. 105, 348–363 (2018).
Novák, P., Neumann, P., Pech, J., Steinhaisl, J. & Macas, J. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29, 792–793 (2013).
Pellicer, J. & Leitch, I. J. The Plant DNA C-values database (release 7.1): an updated online repository of plant genome size data for comparative studies. New Phytol. 226, 301–305 (2019).
Ickert-Bond, S. M. et al. Polyploidy in gymnosperms—insights into the genomic and evolutionary consequences of polyploidy in Ephedra. Mol. Phyl. Evol. 147, 106786 (2020).
Pellicer, J. & Leitch, I. J. in Molecular Plant Taxonomy Vol. 1115 (ed. Besse, P.) 279–307 (Humana Press, 2014).
Ferrari, S. & Cribari-Neto, F. Beta regression for modelling rates and proportions. J. Appl. Stat. 31, 799–815 (2004).
Cribari-Neto, F. & Zeileis, A. Beta Regression in R. J. Stat. Softw. 34, 1–24 (2010).
Smithson, M. & Verkuilen, J. A better lemon squeezer? Maximum-likelihood regression with beta-distributed dependent variables. Psychol. Meth. 11, 54–71 (2006).
Durka, W. & Michalski, S. G. Daphne: a dated phylogeny of a large European flora for phylogenetically informed ecological analyses. Ecology 93, 2297–2297 (2012).
Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
Rambaut, A. FigTree version 1.4.3 http://tree.bio.ed.ac.uk/software/figtree (2012).
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: Linear and Nonlinear Mixed Effects Models. R Package version 3.1 http://cran.r-project.org/package=nlme (2017).
Contrasting distributions and expression characteristics of transcribing repeats in Setaria viridis
Cytomolecular diversity among Vigna Savi (Leguminosae) subgenera
Intragenomic rDNA variation - the product of concerted evolution, mutation, or something in between?
The ecology of palm genomes: repeat-associated genome size expansion is constrained by aridity